The evolution of an individual-like dispersive stage in colonial siphonophores.

Reproduction in sedentary colonial species often involves the release of a dispersive stage, such as a larva or individual zooids, which promotes gene flow and enables range expansion. In some species of pelagic colonial siphonophores (Cnidaria: Hydrozoa), reproduction occurs through colony fragmentation, an evolutionarily unique strategy in which the entire terminal zooid cluster, instead of releasing individual reproductive zooids, detaches as a dispersive unit known as a eudoxid. Although composed of multiple functionally specialized zooids, the eudoxid behaves as a single individual, suggesting an elusive evolutionary transition in individuality. The mechanisms and evolutionary origins of eudoxid production, however, remain unknown. Using live imaging, immunohistochemistry, and pharmacological inhibition, we provide a mechanistic understanding of eudoxid formation. We demonstrate that eudoxid release is controlled by a dedicated muscle and involves tissue remodeling, resulting in the formation of a physiologically integrated dispersive unit with distinct behaviors. Our analyses suggest that eudoxids evolved once, through the concomitant reorganization of colony architecture and the evolution of zooid structures. We also show that eudoxids and their parental colonies often have different distributions, suggesting niche partitioning. These findings reveal how muscle evolution and structural modifications of the colony enabled the emergence of a unique, individual-like dispersive stage, contributing to the ecological success of siphonophores in marine environments.